Aim Our aim was to examine gracile capuchin (Cebus) and robust capuchin monkey (Sapajus) diversification, with a focus on recent Sapajus expansion within Amazonia. We wanted to reconstruct the biogeographical history of the clade using statistical methods that model lineages' occupation of different regions over time in order to evaluate recently proposed 'Out of Amazonia' and 'Reinvasion of Amazonia' hypotheses as alternative explanations for the extensive geographical overlap between reciprocally monophyletic gracile (Cebus) and robust (Sapajus) capuchin monkeys.Location Central and South America.Methods We reconstructed a time-calibrated molecular phylogeny for capuchins under Bayesian inference from three mitochondrial genes. We then categorized 12 capuchin clades across four Neotropical centres of endemism and reconstructed the biogeographical history of the capuchin radiation using six models implemented in 'BioGeoBEARS'. We performed a phylogeographical analysis for a robust capuchin clade that spans the Atlantic Forest, Cerrado, Caatinga and Amazonia. ResultsWe find support for a late Miocene vicariant Cebus-Sapajus divergence and a Pleistocene Sapajus invasion of Amazonia from the Atlantic Forest. Our new analyses confirm Sapajus diversified first in the Atlantic Forest, with subsequent range expansion into widespread sympatry with Cebus in Amazonia, as well as multiple expansions into drier savanna-like habitats. We do not find mitochondrial molecular congruence with morphological species distinctions for Sapajus flavius, S. cay, S. macrocephalus, S. libidinosus and S. apella; instead, these five morphological types together form a single widespread clade (Bayesian posterior probability = 1) with geographical substructure and shared ancestry during the Pleistocene.Main conclusions Our results support vicariance dividing ancestral capuchin populations in Amazonia versus the Atlantic Forest, and a Pleistocene 'Amazonian invasion' by Sapajus to explain the present-day sympatry of Cebus and Sapajus.

Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provided support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidinosus as sister species; however, S. apella, S. macrocephalus, and S. cay individuals were recovered in two geographic clades, from northeastern and southwestern Amazon, rather than clustering by currently defined morphospecies. STRUCTURE analysis of population clustering revealed widespread admixture among Sapajus populations within the Amazon and even into the Cerrado and Atlantic Forest. Difficulty in assigning species by morphology may be a result of widespread population admixture facilitated through frequent movement across major rivers and even ecosystems by robust capuchin monkeys.

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